Xue Yu-Xiao, Chen Yi-Jun, Qin Mei-Zhen, Shang Fan-Fan, Lu Yi-Ting, Sun Yu-Hao, Bian Liu-Guan, Zhang Ao, Yu Yang, Ding Chun-Yong
Department of Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200020, China.
Shanghai Frontiers Science Center of Drug Target Identification and Delivery, National Key Laboratory of Innovative Immunotherapy, School of Pharmaceutical Sciences, Shanghai Jiao Tong University, Shanghai, 200240, China.
Acta Pharmacol Sin. 2025 Apr 8. doi: 10.1038/s41401-025-01540-8.
Neuroinflammation, a significant contributor to secondary brain injury, plays a critical role in the pathological process and prognosis of intracerebral haemorrhage (ICH). Thus, developing interventions to mitigate secondary neuroimmune deterioration is of paramount importance. Currently, no effective immunomodulatory drugs are available for ICH. The cyclic GMP-AMP synthase (cGAS)-stimulator of interferon genes (STING) pathway is a recently identified innate immune-sensing pathway primarily expressed in microglia within the central nervous system (CNS) that has been implicated in the pathophysiology of various neurological diseases. In this study we investigated the role of cGAS-STING pathway in ICH. A collagenase model of ICH was established in mice. Brain tissues were collected on D1 or D3 post-ICH. We observed a significant increase in double-stranded (dsDNA) levels and activation of the cGAS-STING pathway in the perihaematomal region of ICH mice. Administration of a blood brain barrier-permeable STING antagonist H151 (10 mg/kg, i.p.) significantly decreased cell apoptosis, alleviated hematoma growth, and improved motor impairments in ICH mice, accompanied by inhibiting the STING pathway in microglia, reducing production/release of the cGAS-STING pathway downstream inflammatory factors, NLRP3 inflammasome activation and gasdermin D (GSDMD)-induced microglial pyroptosis. Microglial Sting conditional knockout significantly mitigated ICH-induced neuroinflammatory responses, pathological damage and motor dysfunction. These results suggest that the microglial STING pathway promotes brain pathological damage and behavioural defects in ICH mice by activating the NLRP3 inflammasome and microglial pyroptosis. The STING pathway may serve as a potential therapeutic target for ICH-induced secondary brain injury.
神经炎症是继发性脑损伤的重要促成因素,在脑出血(ICH)的病理过程和预后中起关键作用。因此,开发减轻继发性神经免疫恶化的干预措施至关重要。目前,尚无有效的免疫调节药物可用于ICH治疗。环磷酸鸟苷-腺苷酸合成酶(cGAS)-干扰素基因刺激因子(STING)通路是最近发现的一种天然免疫传感通路,主要在中枢神经系统(CNS)的小胶质细胞中表达,与多种神经疾病的病理生理学有关。在本研究中,我们调查了cGAS-STING通路在ICH中的作用。在小鼠中建立了ICH胶原酶模型。在ICH后第1天或第3天收集脑组织。我们观察到ICH小鼠血肿周围区域双链(dsDNA)水平显著升高,cGAS-STING通路激活。给予血脑屏障可通透的STING拮抗剂H151(10 mg/kg,腹腔注射)可显著降低ICH小鼠的细胞凋亡,减轻血肿生长,并改善运动障碍,同时抑制小胶质细胞中的STING通路,减少cGAS-STING通路下游炎症因子的产生/释放、NLRP3炎性小体激活和gasdermin D(GSDMD)诱导的小胶质细胞焦亡。小胶质细胞Sting条件性敲除显著减轻了ICH诱导的神经炎症反应、病理损伤和运动功能障碍。这些结果表明,小胶质细胞STING通路通过激活NLRP3炎性小体和小胶质细胞焦亡促进ICH小鼠的脑病理损伤和行为缺陷。STING通路可能是ICH诱导的继发性脑损伤的潜在治疗靶点。